Conceptual Framework to Guide Early Diagnosis Programs for Symptomatic Cancer as Part of Global Cancer Control

Minjoung Monica Koo, Karla Unger-Saldaña, Amos D Mwaka, Marilys Corbex, Ophira Ginsburg, Fiona M Walter, Natalia Calanzani, Jennifer Moodley, Greg P Rubin, Georgios Lyratzopoulos, Minjoung Monica Koo, Karla Unger-Saldaña, Amos D Mwaka, Marilys Corbex, Ophira Ginsburg, Fiona M Walter, Natalia Calanzani, Jennifer Moodley, Greg P Rubin, Georgios Lyratzopoulos

Abstract

Diagnosing cancer earlier can enable timely treatment and optimize outcomes. Worldwide, national cancer control plans increasingly encompass early diagnosis programs for symptomatic patients, commonly comprising awareness campaigns to encourage prompt help-seeking for possible cancer symptoms and health system policies to support prompt diagnostic assessment and access to treatment. By their nature, early diagnosis programs involve complex public health interventions aiming to address unmet health needs by acting on patient, clinical, and system factors. However, there is uncertainty regarding how to optimize the design and evaluation of such interventions. We propose that decisions about early diagnosis programs should consider four interrelated components: first, the conduct of a needs assessment (based on cancer-site-specific statistics) to identify the cancers that may benefit most from early diagnosis in the target population; second, the consideration of symptom epidemiology to inform prioritization within an intervention; third, the identification of factors influencing prompt help-seeking at individual and system level to support the design and evaluation of interventions; and finally, the evaluation of factors influencing the health systems' capacity to promptly assess patients. This conceptual framework can be used by public health researchers and policy makers to identify the greatest evidence gaps and guide the design and evaluation of local early diagnosis programs as part of broader cancer control strategies.

Conflict of interest statement

Karla Unger-Saldaña

Honoraria: Roche

Travel, Accommodations, Expenses: Roche

Jennifer Moodley

Research Funding: Discovery Health, GlaxoSmithKline

No other potential conflicts of interest were reported.

Figures

FIG 1
FIG 1
Conceptual framework for the design and evaluation of early diagnosis programs for cancer.

References

    1. World Health Organization : WHO report on cancer: setting priorities, investing wisely and providing care for all. Geneva, 2020.
    1. World Health Organization : Noncommunicable diseases. 2020.
    1. Balogh E, Patlak M, Nass SJ, et al. : Cancer Care in Low-Resource Areas. Washington, DC, National Academies Press, 2016.
    1. Ott JJ, Ullrich A, Miller AB: The importance of early symptom recognition in the context of early detection and cancer survival. Eur J Cancer 45:2743-2748, 2009
    1. Laudicella M, Walsh B, Burns E, et al. : Cost of care for cancer patients in England: Evidence from population-based patient-level data. Br J Cancer 114:1286-1292, 2016
    1. Tørring ML, Murchie P, Hamilton W, et al. : Evidence of advanced stage colorectal cancer with longer diagnostic intervals: A pooled analysis of seven primary care cohorts comprising 11 720 patients in five countries. Br J Cancer 117:888-897, 2017
    1. Neal RD, Tharmanathan P, France B, et al. : Is increased time to diagnosis and treatment in symptomatic cancer associated with poorer outcomes? Systematic review. Br J Cancer 112:S92-S107, 2015
    1. Tørring ML, Falborg AZ, Jensen H, et al. : Advanced‐stage cancer and time to diagnosis: An International Cancer Benchmarking Partnership (ICBP) cross‐sectional study. Eur J Cancer Care (Engl) 28:e13100, 2019
    1. Koo MM, Swann R, McPhail S, et al. : Presenting symptoms of cancer and stage at diagnosis: Evidence from a cross-sectional, population-based study. Lancet Oncol 2045:1-7, 2019
    1. Sandager M, Jensen H, Lipczak H, et al. : Cancer patients' experiences with urgent referrals to cancer patient pathways. Eur J Cancer Care (Engl) e12927, 2018
    1. Mendonca SC, Abel G, Saunders CL, et al. : Pre-referral general practitioner consultations and subsequent experience of cancer care: Evidence from the English Cancer Patient Experience Survey. Eur J Cancer Care (Engl) 25:478-490, 2016
    1. World Health Organization : Guide to cancer: early diagnosis. 2017.
    1. Elliss-Brookes L, McPhail S, Ives A, et al. : Routes to diagnosis for cancer—Determining the patient journey using multiple routine data sets. Br J Cancer 107:1220-1226, 2012
    1. Sarma EA, Kobrin SC, Thompson MJ: A proposal to improve the early diagnosis of symptomatic cancers in the United States. Cancer Prev Res 13:715–720, 2020
    1. Ilbawi AM, Anderson BO: Cancer in global health: How do prevention and early detection strategies relate?. Sci Transl Med 7:278cm1, 2015
    1. Sankaranarayanan R, Boffetta P: Research on cancer prevention, detection and management in low- and medium-income countries. Ann Oncol 21:1935–1943, 2010
    1. Corbex M, Burton R, Sancho-Garnier H: Breast cancer early detection methods for low and middle income countries, a review of the evidence. Breast 21:428-434, 2012
    1. Devi BCR, Tang TS, Corbex M: Reducing by half the percentage of late-stage presentation for breast and cervix cancer over 4 years: A pilot study of clinical downstaging in Sarawak, Malaysia. Ann Oncol 18:1172-1176, 2007
    1. Public Health England : Be clear on cancer—Current campaigns. 2016.
    1. Cancer Research UK : About be clear on cancer. Early diagnosis Act. 2014.
    1. Forbes LJL, Warburton F, Richards MA, et al. : Risk factors for delay in symptomatic presentation: A survey of cancer patients. Br J Cancer 111:581-588, 2014
    1. Ironmonger L, Ohuma E, Ormiston-Smith N, et al. : An evaluation of the impact of large-scale interventions to raise public awareness of a lung cancer symptom. Br J Cancer 112:207-216, 2015
    1. Moffat J, Bentley A, Ironmonger L, et al. : The impact of national cancer awareness campaigns for bowel and lung cancer symptoms on sociodemographic inequalities in immediate key symptom awareness and GP attendances. Br J Cancer 112:S14-S21, 2015
    1. Public Health England : Be clear on cancer evaluation. NCRAS. 2019.
    1. Lai J, Mak V, Bright CJ, et al. : Reviewing the impact of 11 national be clear on cancer public awareness campaigns, England 2012‐2016: A synthesis of published evaluation results. Int J Cancer 10.1002/ijc.33277 [epub ahead of print on September 1, 2020]
    1. Schliemann D, Donnelly M, Dahlui M, et al. : The “Be Cancer Alert Campaign”: Protocol to evaluate a mass media campaign to raise awareness about breast and colorectal cancer in Malaysia. BMC Cancer 18:881, 2018
    1. Schliemann D, Htay MNN, Dahlui M, et al. : Impact of a mass media campaign on breast cancer symptoms awareness and screening uptake in Malaysia: Findings from a quasi-experimental study. BMJ Open 10:e036503, 2020
    1. Schliemann D, Paramasivam D, Dahlui M, et al. : Change in public awareness of colorectal cancer symptoms following the Be Cancer Alert Campaign in the multi-ethnic population of Malaysia. BMC Cancer 20:252, 2020
    1. AfrOx : Early diagnosis and prevention. 2011.
    1. Cancer Australia : Campaigns and events. 2016.
    1. Yaqub F: Punjab's cancer awareness campaign. Lancet Oncol 14:e92, 2013
    1. Puckett MC, Townsend JS, Gelb CA, et al. : Ovarian cancer knowledge in women and providers following education with inside knowledge campaign materials. J Cancer Educ 33:1285-1293, 2018
    1. World Wide Breast Cancer : Know your lemons. 2016.
    1. Allemani C, Matsuda T, Di Carlo V, et al. : Global surveillance of trends in cancer survival 2000–14 (CONCORD-3): Analysis of individual records for 37 513 025 patients diagnosed with one of 18 cancers from 322 population-based registries in 71 countries. Lancet 391:1023-1075, 2018
    1. Arnold M, Rutherford MJ, Bardot A, et al. : Progress in cancer survival, mortality, and incidence in seven high-income countries 1995–2014 (ICBP SURVMARK-2): A population-based study. Lancet Oncol 20:1493-1505, 2019
    1. Richards M, Thorlby R, Fisher R, et al. : Unfinished business: An assessment of the national approach to improving cancer services in England 1995–2015. London. 2018.
    1. NICE : Suspected cancer: recognition and referral. Cardiff. 2015.
    1. NHS England : Cancer waiting times. 2020.
    1. Vedsted P, Olesen F: A differentiated approach to referrals from general practice to support early cancer diagnosis—The Danish three-legged strategy. Br J Cancer 112:S65-S69, 2015
    1. Jensen H, Tørring ML, Vedsted P: Prognostic consequences of implementing cancer patient pathways in Denmark: A comparative cohort study of symptomatic cancer patients in primary care. BMC Cancer 17:627, 2017
    1. Walters S, Benitez-Majano S, Muller P, et al. : Is England closing the international gap in cancer survival?. Br J Cancer 113:848-860, 2015
    1. Round T, Gildea C, Ashworth M, et al. : Association between use of urgent suspected cancer referral and mortality and stage at diagnosis: A 5-year national cohort study. Br J Gen Pract 70:e389-e398, 2020
    1. Herbert A, Abel GA, Winters S, et al. : Cancer diagnoses after emergency GP referral or A&E attendance in England: Determinants and time trends in Routes to Diagnosis data, 2006-2015. Br J Gen Pract 69:e724-e730, 2019
    1. Zhou Y, Abel GA, Hamilton W, et al. : Diagnosis of cancer as an emergency: A critical review of current evidence. Nat Rev Clin Oncol 14:45-56, 2017
    1. Prades J, Espinàs Ja, Font R, et al. : Implementing a cancer fast-track programme between primary and specialised care in Catalonia (Spain): A mixed methods study. Br J Cancer 105:753-759, 2011
    1. Harrison AJ, Foot CS: Targets and prioritization: The case of cancer in the English NHS. Qual Prim Care 20:125-129, 2012
    1. New Zealand Guidelines Group (NZGG) . 2009. Suspected Cancer in Primary Care: Guidelines for investigation, referral and reducing ethnic disparities. Wellington:New Zealand Guidelines Group.
    1. Valentin-Lopez B, Ferrandiz-Santos J, Blasco-Amaro J-A, et al. : Assessment of a rapid referral pathway for suspected colorectal cancer in Madrid. Fam Pract 29:182-188, 2012
    1. Scott SE, Walter FM, Webster A, et al. : The model of pathways to treatment: Conceptualization and integration with existing theory. Br J Health Psychol 18:45-65, 2013
    1. Weller D, Vedsted P, Rubin G, et al. : The Aarhus statement: Improving design and reporting of studies on early cancer diagnosis. Br J Cancer 106:1262-1267, 2012
    1. Walter F, Webster A, Scott S, et al. : The Andersen model of total patient delay: A systematic review of its application in cancer diagnosis. J Health Serv Res Policy 17:110-118, 2012
    1. Craig P, Dieppe P, Macintyre S, et al. : Developing and evaluating complex interventions: The new Medical Research Council guidance. BMJ 337:a1655, 2008
    1. Campbell M, Fitzpatrick R, Haines A, et al. : Framework for design and evaluation of complex interventions to improve health Framework for trials of complex interventions. Br Med J 321:694-696, 2000
    1. Campbell NCN, Murray E, Darbyshire J, et al. : Designing and evaluating complex interventions to improve health care. Br Med J 334:455-459, 2007
    1. Ogilvie D, Adams J, Bauman A, et al. : Using natural experimental studies to guide public health action: Turning the evidence-based medicine paradigm on its head. J Epidemiol Community Health 74:203-208, 2019
    1. Donnelly C, Cairnduff V, Chen JJ, et al. : The completeness and timeliness of cancer registration and the implications for measuring cancer burden. Cancer Epidemiol 49:101-107, 2017
    1. Hamilton W, Stapley S, Campbell C, et al. : For which cancers might patients benefit most from expedited symptomatic diagnosis? Construction of a ranking order by a modified Delphi technique. BMC Cancer 15:820, 2015
    1. Koo MM, Hamilton W, Walter FM, et al. : Symptom signatures and diagnostic timeliness in cancer patients: A review of current evidence. Neoplasia 20:165-174, 2017
    1. Verheij RA, Curcin V, Delaney BC, et al. : Possible sources of bias in primary care electronic health record data use and reuse. J Med Internet Res 20:e185, 2018
    1. Hamilton W, Peters TJ, Bankhead C, et al. : Risk of ovarian cancer in women with symptoms in primary care: population based case-control study. BMJ 339:b2998, 2009
    1. Walker S, Hyde C, Hamilton W: Risk of breast cancer in symptomatic women in primary care: a case-control study using electronic records. Br J Gen Pract 64:e788-e793, 2014
    1. Ewing M, Naredi P, Zhang C, et al. : Clinical features of patients with non-metastatic lung cancer in primary care: A case-control study. BJGP Open 2:bjgpopen18X101397, 2018
    1. Lawrenson R, Logie J, Marks C: Risk of colorectal cancer in general practice patients presenting with rectal bleeding, change in bowel habit or anaemia. Eur J Cancer Care (Engl) 15:267-271, 2006
    1. Jones R, Latinovic R, Charlton J, et al. : Alarm symptoms in early diagnosis of cancer in primary care: Cohort study using General Practice Research Database. BMJ 334:1040, 2007
    1. Shephard E, Neal R, Rose P, et al. : Clinical features of kidney cancer in primary care: A case-control study using primary care records. Br J Gen Pract 63:e250-e255, 2013
    1. Collins GS, Altman DG: Identifying patients with undetected gastro-oesophageal cancer in primary care: External validation of QCancer® (Gastro-Oesophageal). Eur J Cancer 49:1040-1048, 2012
    1. Hamilton W, Sharp DJ, Peters TJ, et al. : Clinical features of prostate cancer before diagnosis: A population-based, case-control study. Br J Gen Pract 56:756-762, 2006
    1. Hamilton W, Barrett J, Stapley S, et al. : Clinical features of metastatic cancer in primary care: A case-control study using medical records. Br J Gen Pract 65:e516-e522, 2015
    1. Hamilton W, Peters TJ, Round A, et al. : What are the clinical features of lung cancer before the diagnosis is made? A population based case-control study. Thorax 60:1059-1065, 2005
    1. Walker S, Hamilton W: Risk of cervical cancer in symptomatic women aged ≥40 in primary care: A case-control study using electronic records. Eur J Cancer Care (Engl) 63:e12706, 2017
    1. Stapley S, Peters TJ, Neal RD, et al. : The risk of oesophago-gastric cancer in symptomatic patients in primary care: A large case-control study using electronic records. Br J Cancer 108:25-31, 2013
    1. Astin M, Griffin T, Neal RD, et al. : The diagnostic value of symptoms for colorectal cancer in primary care: A systematic review. Br J Gen Pract 61:231-243, 2011
    1. Stapley S, Peters TJ, Neal RD, et al. : The risk of pancreatic cancer in symptomatic patients in primary care: A large case-control study using electronic records. Br J Cancer 106:1940-1944, 2012
    1. Shephard EA, Stapley S, Neal RD, et al. : Clinical features of bladder cancer in primary care. Br J Gen Pract 62:598-604, 2012
    1. Shephard EA, Neal RD, Rose P, et al. : Quantifying the risk of multiple myeloma from symptoms reported in primary care patients: A large case-control study using electronic records. Br J Gen Pract 65:e106-e113, 2015
    1. Forbes LJL, Simon AE, Warburton F, et al. : Differences in cancer awareness and beliefs between Australia, Canada, Denmark, Norway, Sweden and the UK (the International Cancer Benchmarking Partnership): Do they contribute to differences in cancer survival? Br J Cancer 108:292-300, 2013
    1. Menon U Vedsted P Zalounina Falborg A et al. :. Time intervals and routes to diagnosis for lung cancer in 10 jurisdictions: cross-sectional study findings from the International Cancer Benchmarking Partnership (ICBP) BMJ Open 2019;9:e025895. doi: 10.1136/bmjopen-2018-025895
    1. Jensen H, Tørring ML, Olesen F, et al. : Cancer suspicion in general practice, urgent referral and time to diagnosis: A population-based GP survey and registry study. BMC Cancer 14:636, 2014
    1. Forster AS, Renzi C, Lyratzopoulos G: Diagnosing cancer in patients with “non-alarm” symptoms: Learning from diagnostic care innovations in Denmark. Cancer Epidemiol 54:101-103, 2018
    1. Fuller E, Fitzgerald K, Hiom S, et al. : Accelerate, coordinate, evaluate programme: A new approach to cancer diagnosis. Br J Gen Pract 66:176-177, 2016
    1. Chapman D, Poirier V, Vulkan D, et al. : First results from five multidisciplinary diagnostic centre (MDC) projects for non-specific but concerning symptoms, possibly indicative of cancer. Br J Cancer 123:722-729, 2020
    1. Nicholson BD, Oke J, Friedemann Smith C, et al. : The Suspected CANcer (SCAN) pathway: Protocol for evaluating a new standard of care for patients with non-specific symptoms of cancer. BMJ Open 8:1-8, 2018
    1. Sewell B, Jones M, Gray H, et al. : Rapid cancer diagnosis for patients with vague symptoms: A cost-effectiveness study. Br J Gen Pract 70:e186-e192, 2020
    1. Stubbings S, Robb K, Waller J, et al. : Development of a measurement tool to assess public awareness of cancer. Br J Cancer 101:S13-S17, 2009. (suppl)
    1. Robb K, Stubbings S, Ramirez AJ, et al. : Public awareness of cancer in Britain: A population-based survey of adults. Br J Cancer 101:S18–S23, 2009
    1. Simon AE, Forbes LJL, Boniface D, et al. : An international measure of awareness and beliefs about cancer: Development and testing of the ABC. BMJ Open 2:e001758, 2012
    1. Moodley J, Scott SE, Mwaka AD, et al. : Development and validation of the African Women Awareness of CANcer (AWACAN) tool for breast and cervical cancer. PLoS One 14:e0220545, 2019
    1. Su TT, Goh JY, Tan J, et al. : Level of colorectal cancer awareness: A cross sectional exploratory study among multi-ethnic rural population in Malaysia. BMC Cancer 13:376, 2013
    1. Rendle KA, Sarma EA, Quaife SL, et al. : Cancer symptom recognition and anticipated delays in seeking care among U.S. adults. Am J Prev Med 57:e1-e9, 2019
    1. Koo MM, von Wagner C, Abel GA, et al. : The nature and frequency of abdominal symptoms in cancer patients and their associations with time to help-seeking: Evidence from a national audit of cancer diagnosis. J Public Health (Bangkok) 40:e388-e395, 2018
    1. Whitaker KL, Scott SE, Wardle J: Applying symptom appraisal models to understand sociodemographic differences in responses to possible cancer symptoms: A research agenda. Br J Cancer 112:S27-S34, 2015. (suppl)
    1. McCutchan GM, Wood F, Edwards A, et al. : Influences of cancer symptom knowledge, beliefs and barriers on cancer symptom presentation in relation to socioeconomic deprivation: A systematic review. BMC Cancer 15:1000, 2015
    1. Humphrys E, Burt J, Rubin G, et al. : The influence of health literacy on the timely diagnosis of symptomatic cancer: A systematic review. Eur J Cancer Care (Engl) 28:e12920, 2019
    1. Mwaka AD, Okello ES, Wabinga H: Perceptions and beliefs of lay people from northern Uganda regarding surgery for diagnosis and treatment of cervical cancer. Psychooncology 27:1965-1970, 2018
    1. MacArtney J, Malmström M, Overgaard Nielsen T, et al. : Patients' initial steps to cancer diagnosis in Denmark, England and Sweden: What can a qualitative, cross-country comparison of narrative interviews tell us about potentially modifiable factors? BMJ Open 7:e018210, 2017
    1. Unger-Saldaña K, Infante-Castañeda CB: Breast cancer delay: A grounded model of help-seeking behaviour. Soc Sci Med 72:1096-1104, 2011
    1. Moodley J, Cairncross L, Naiker T, et al. : From symptom discovery to treatment—Women's pathways to breast cancer care: a cross-sectional study. BMC Cancer 18:312, 2018
    1. Foerster M, McKenzie F, Zietsman A, et al. : Dissecting the journey to breast cancer diagnosis in sub‐Saharan Africa: Findings from the multicountry ABC‐DO cohort study. Int J Cancer 10.1002/ijc.33209 [epub ahead of print on July 14, 2020]
    1. Smith LK, Pope C, Botha JL: Patients' help-seeking experiences and delay in cancer presentation: A qualitative synthesis. Lancet 366:825-831, 2005
    1. Mullins MA, Peres LC, Alberg AJ, et al. : Perceived discrimination, trust in physicians, and prolonged symptom duration before ovarian cancer diagnosis in the African American Cancer Epidemiology Study. Cancer 125:4442-4451, 2019
    1. Lyratzopoulos G, Liu MP-H, Abel GA, et al. : The Association between fatalistic beliefs and late stage at diagnosis of lung and colorectal cancer. Cancer Epidemiol Biomarkers Prev 24:720-726, 2015
    1. Anakwenze C, Bhatia R, Rate W, et al. : Factors related to advanced stage of cancer presentation in Botswana. J Glob Oncol 1-9, 2018.
    1. Shahid S, Teng T-HK, Bessarab D, et al. : Factors contributing to delayed diagnosis of cancer among Aboriginal people in Australia: A qualitative study: Table 1. BMJ Open 6:e010909, 2016
    1. Youl P, Aitken J, Turrell G, et al. : The impact of rurality and disadvantage on the diagnostic interval for breast cancer in a large population-based study of 3202 women in Queensland, Australia. Int J Environ Res Public Health 13:1156, 2016
    1. Dianatinasab M, Fararouei M, Mohammadianpanah M, et al. : Impact of social and clinical factors on diagnostic delay of breast cancer. Medicine (Baltimore) 95:e4704, 2016
    1. Berraho M, Obtel M, Bendahhou K, et al. : Sociodemographic factors and delay in the diagnosis of cervical cancer in Morocco. Pan Afr Med J 12:1-8, 2012
    1. Unger-Saldaña K: Challenges to the early diagnosis and treatment of breast cancer in developing countries. World J Clin Oncol 5:465, 2014
    1. Ginsburg O, Yip C, Brooks A, et al. : Breast cancer early detection: A phased approach to implementation. Cancer 126:2379-2393, 2020
    1. Horton S, Camacho Rodriguez R, Anderson BO, et al. : Health system strengthening: Integration of breast cancer care for improved outcomes. Cancer 126:2353-2364, 2020
    1. Rubin G, Berendsen A, Crawford SM, et al. : The expanding role of primary care in cancer control. Lancet Oncol 16:1231-1272, 2015
    1. World Health Organization : WHO list of priority medical devices for cancer management. 2017.
    1. Rubin G, Walter F, Emery J, et al. : Reimagining the diagnostic pathway for gastrointestinal cancer. Nat Rev Gastroenterol Hepatol 15:181-188, 2018
    1. van Melle M, Yep Manzano SI, Wilson H, et al. : Faecal immunochemical test to triage patients with abdominal symptoms for suspected colorectal cancer in primary care: Review of international use and guidelines. Fam Pract, 2020.
    1. Westwood M, Lang S, Armstrong N, et al. : Faecal immunochemical tests (FIT) can help to rule out colorectal cancer in patients presenting in primary care with lower abdominal symptoms: A systematic review conducted to inform new NICE DG30 diagnostic guidance. BMC Med 15:189, 2017
    1. Nicholson BD, James T, Paddon M, et al. : Faecal immunochemical testing for adults with symptoms of colorectal cancer attending English primary care: A retrospective cohort study of 14 487 consecutive test requests. Aliment Pharmacol Ther 1-11, 2020.
    1. McKenzie F, Zietsman A, Galukande M, et al. : Drivers of advanced stage at breast cancer diagnosis in the multicountry African breast cancer—Disparities in outcomes (ABC-DO) study. Int J Cancer 142:1568-1579, 2018
    1. Chibwesha C, Pinder LF, Musonda A, et al. : A comprehensive assessment of breast and cervical cancer control infrastructure in Zambia. J Cancer Policy 13:24-29, 2017
    1. Songiso M, Pinder LF, Munalula J, et al. : Minimizing delays in the breast cancer pathway by integrating breast specialty care services at the primary health care level in Zambia. JCO Glob Oncol 859-865, 2020
    1. Unger-Saldaña K, Fitch-Picos K, Villarreal-Garza C: Breast cancer diagnostic delays among young Mexican women are associated with a lack of suspicion by health care providers at first presentation. J Glob Oncol 5:1-12, 2019
    1. Pace LE, Dusengimana JMV, Shulman LN, et al. : Cluster randomized trial to facilitate breast cancer early diagnosis in a rural district of Rwanda. J Glob Oncol 1-13, 2019.
    1. Unger-Saldaña K, Miranda A, Zarco-Espinosa G, et al. : Health system delay and its effect on clinical stage of breast cancer: Multicenter study. Cancer 121:2198-2206, 2015
    1. Mwaka AD, Okello ES, Wabinga H, et al. : Symptomatic presentation with cervical cancer in Uganda: A qualitative study assessing the pathways to diagnosis in a low-income country. BMC Womens Health 15:15, 2015
    1. Sardi A, Orozco-Urdaneta M, Velez-Mejia C, et al. : Overcoming barriers in the implementation of programs for breast and cervical cancers in Cali, Colombia: A pilot model. J Glob Oncol 5:1-9, 2019
    1. Morgan GW, Foster K, Healy B, et al. : Improving health and cancer services in low-resource countries to attain the sustainable development goals target 3.4 for noncommunicable diseases. J Glob Oncol 1-11, 2018.
    1. Atun R, Cavalli F: The global fight against cancer: Challenges and opportunities. Lancet 391:412-413, 2018
    1. Swann R, McPhail S, Witt J, et al. : Diagnosing cancer in primary care: Results from the National Cancer Diagnosis Audit. Br J Gen Pract 68:e63-e72, 2018
    1. Proctor E, Silmere H, Raghavan R, et al. : Outcomes for implementation research: Conceptual distinctions, measurement challenges, and research agenda. Adm Policy Ment Heal Ment Heal Serv Res 38:65-76, 2011
    1. Michie S, van Stralen MM, West R: The behaviour change wheel: A new method for characterising and designing behaviour change interventions. Implement Sci 6:42, 2011
    1. Chambers D, Vinson C, Norton W: Advancing the Science of Implementation Across the Cancer Continuum (ed 1). Oxford University Press, 2018.
    1. Peters DH, Adam T, Alonge O, et al. : Republished research: Implementation research: What it is and how to do it. Br J Sports Med 48:731-736, 2014
    1. Sivaram S, Sanchez MA, Rimer BK, et al. : Implementation science in cancer prevention and control: A framework for research and programs in low- and middle-income countries. Cancer Epidemiol Biomarkers Prev 23:2273-2284, 2014
    1. Rositch AF, Unger‐Saldaña K, DeBoer RJ, et al. : The role of dissemination and implementation science in global breast cancer control programs: Frameworks, methods, and examples. Cancer 126:2394-2404, 2020
    1. Stirman SW, Miller CJ, Toder K, et al. : Development of a framework and coding system for modifications and adaptations of evidence-based interventions. Implement Sci 8:65, 2013
    1. May C, Finch T: Implementing, embedding, and integrating practices: An outline of normalization process theory. Sociology 43:535-554, 2009
    1. McCutchan G, Smits S, Ironmonger L, et al. : Evaluation of a national lung cancer symptom awareness campaign in Wales. Br J Cancer 122:491-497, 2020
    1. Smits S, McCutchan G, Wood F, et al. : Development of a behavior change intervention to encourage timely cancer symptom presentation among people living in deprived communities using the behavior change wheel. Ann Behav Med, 2016.
    1. Toftegaard BS, Bro F, Vedsted P: A geographical cluster randomised stepped wedge study of continuing medical education and cancer diagnosis in general practice. Implement Sci 9:159, 2014
    1. Dikomitis L, Green T, Macleod U: Embedding electronic decision-support tools for suspected cancer in primary care: A qualitative study of GPs' experiences. Prim Health Care Res Dev 16:548-555, 2015
    1. Chiang PPC, Glance D, Walker J, et al. : Implementing a QCancer risk tool into general practice consultations: An exploratory study using simulated consultations with Australian general practitioners. Br J Cancer 112:S77-S83, 2015
    1. Green T, Martins T, Hamilton W, et al. : Exploring GPs' experiences of using diagnostic tools for cancer: A qualitative study in primary care. Fam Pract 32:101-105, 2015
    1. Rosendal M, Jarbøl DE, Pedersen AF, et al. : Multiple perspectives on symptom interpretation in primary care research. BMC Fam Pract 14:167, 2013
    1. Emery JD, Gray V, Walter FM, et al. : The improving rural cancer outcomes trial: A cluster-randomised controlled trial of a complex intervention to reduce time to diagnosis in rural cancer patients in Western Australia. Br J Cancer 117:1459-1469, 2017
    1. Dahl TL, Vedsted P, Jensen H: The effect of standardised cancer pathways on Danish cancer patients' dissatisfaction with waiting time. Dan Med J 64, 2017
    1. Rubin G, Gildea C, Wild S, et al. : Assessing the impact of an English national initiative for early cancer diagnosis in primary care. Br J Cancer 112:S57-S64, 2015. (suppl)
    1. Toftegaard BS, Bro F, Falborg AZ, et al. : Impact of a continuing medical education meeting on the use and timing of urgent cancer referrals among general practitioners—A before-after study. BMC Fam Pract 18:44, 2017
    1. Smith SM, Whitaker KL, Cardy AH, et al. : Validation of self-reported help-seeking, and measurement of the patient interval, for cancer symptoms: An observational study to inform methodological challenges in symptomatic presentation research. Fam Pract 1-7, 2019.
    1. Lyratzopoulos G, Saunders CL, Abel GA, et al. : The relative length of the patient and the primary care interval in patients with 28 common and rarer cancers. Br J Cancer 112:S35-S40, 2015

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